The neurodynamic organization of modality-dependent hallucinations.

The pathophysiology of hallucinations remains mysterious. This research aims to specifically explore the interaction between hallucinations and spontaneous resting-state activity. We used multimodal magnetic resonance imaging during hallucinations occurrence in 20 drug-free adolescents with a "brief psychotic disorder." They were furthermore compared with 20 matched controls at rest or during exteroceptive stimuli. Anatomical and functional symptom-mapping demonstrated reduced cortical thickness and increased blood oxygen level-dependent signal in modality-dependent association sensory cortices during auditory, visual, and multisensory hallucinations. On the contrary, primary-sensory-cortex recruitment was not systematic and was shown to be associated with increased vividness of the hallucinatory experiences. Spatiotemporal activity patterns in the default-mode network (DMN) during hallucinations and symptom-free periods in patients were compared with patterns measured in healthy individuals. A disengagement of the DMN was concomitant to hallucinations, as for exogenous stimulations in healthy participants. Specifically, spatial and temporal instabilities of the DMN correlated with the severity of hallucinations but persisted during symptom-free periods. These results suggest that hallucinatory experiences emerge from a spontaneous DMN withdrawal, providing a convincing model for hallucinations beyond the auditory modality.

[1]  Richard G. Wise,et al.  Neural correlates of the psychedelic state as determined by fMRI studies with psilocybin , 2012, Proceedings of the National Academy of Sciences.

[2]  S. Heckers,et al.  Functional resting-state networks are differentially affected in schizophrenia , 2011, Schizophrenia Research.

[3]  J. Rapoport,et al.  Childhood onset schizophrenia: high rate of visual hallucinations. , 2011, Journal of the American Academy of Child and Adolescent Psychiatry.

[4]  Georg Northoff,et al.  How can the brain's resting state activity generate hallucinations? A ‘resting state hypothesis’ of auditory verbal hallucinations , 2011, Schizophrenia Research.

[5]  G. Barker,et al.  Changes in the Frontotemporal Cortex and Cognitive Correlates in First-Episode Psychosis , 2010, Biological Psychiatry.

[6]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[7]  Rutger Goekoop,et al.  Deactivation of the parahippocampal gyrus preceding auditory hallucinations in schizophrenia. , 2010, The American journal of psychiatry.

[8]  Martijn P. van den Heuvel,et al.  FUNCTIONAL CONNECTIVITY IN SCHIZOPHRENIA , 2010, Schizophrenia Research.

[9]  K. Vogeley,et al.  Resting-state functional network correlates of psychotic symptoms in schizophrenia , 2010, Schizophrenia Research.

[10]  C. Beckmann,et al.  Frontiers in Systems Neuroscience Systems Neuroscience Review Article , 2022 .

[11]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[12]  Manuel Desco,et al.  Gyral and Sulcal Cortical Thinning in Adolescents with First Episode Early-Onset Psychosis , 2009, Biological Psychiatry.

[13]  V. Calhoun,et al.  Changes in the interaction of resting‐state neural networks from adolescence to adulthood , 2009, Human brain mapping.

[14]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

[15]  D. Pins,et al.  Neural functional organization of hallucinations in schizophrenia: Multisensory dissolution of pathological emergence in consciousness , 2009, Consciousness and Cognition.

[16]  S. Debener,et al.  Default-mode brain dysfunction in mental disorders: A systematic review , 2009, Neuroscience & Biobehavioral Reviews.

[17]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[18]  J. Gabrieli,et al.  Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia , 2009, Proceedings of the National Academy of Sciences.

[19]  Philip K. McGuire,et al.  The hallucinating brain: A review of structural and functional neuroimaging studies of hallucinations , 2008, Neuroscience & Biobehavioral Reviews.

[20]  R. Goebel,et al.  Visual target modulation of functional connectivity networks revealed by self‐organizing group ICA , 2008, Human brain mapping.

[21]  R. Kahn,et al.  Auditory verbal hallucinations predominantly activate the right inferior frontal area. , 2008, Brain : a journal of neurology.

[22]  A. Anderson,et al.  Time course of regional brain activation associated with onset of auditory/verbal hallucinations , 2008, British Journal of Psychiatry.

[23]  Rainer Goebel,et al.  Independent component model of the default-mode brain function: combining individual-level and population-level analyses in resting-state fMRI. , 2008, Magnetic resonance imaging.

[24]  S. Petersen,et al.  The maturing architecture of the brain's default network , 2008, Proceedings of the National Academy of Sciences.

[25]  Yuan Zhou,et al.  Functional disintegration in paranoid schizophrenia using resting-state fMRI , 2007, Schizophrenia Research.

[26]  A. David,et al.  The Effect of Long-Acting Risperidone on Working Memory in Schizophrenia: A Functional Magnetic Resonance Imaging Study , 2007, Journal of clinical psychopharmacology.

[27]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[28]  R. Bluhm,et al.  Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. , 2007, Schizophrenia bulletin.

[29]  M. Bar The proactive brain: using analogies and associations to generate predictions , 2007, Trends in Cognitive Sciences.

[30]  V. Calhoun,et al.  Aberrant "default mode" functional connectivity in schizophrenia. , 2007, The American journal of psychiatry.

[31]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[32]  Paul Allen,et al.  Neural correlates of the misattribution of speech in schizophrenia , 2007, British Journal of Psychiatry.

[33]  Scott T. Grafton,et al.  Wandering Minds: The Default Network and Stimulus-Independent Thought , 2007, Science.

[34]  Rainer Goebel,et al.  Classification of fMRI independent components using IC-fingerprints and support vector machine classifiers , 2007, NeuroImage.

[35]  Jamila Andoh,et al.  Left superior temporal gyrus activation during sentence perception negatively correlates with auditory hallucination severity in schizophrenia patients , 2006, Schizophrenia Research.

[36]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[37]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[38]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[39]  Debra A. Gusnard,et al.  Being a self: Considerations from functional imaging , 2005, Consciousness and Cognition.

[40]  Edson Amaro,et al.  Neural correlates of the misattribution of self‐generated speech , 2005, Human brain mapping.

[41]  Thomas Dierks,et al.  The spatiotemporal pattern of auditory cortical responses during verbal hallucinations , 2005, NeuroImage.

[42]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Aapo Hyvärinen,et al.  Independent component analysis of fMRI group studies by self-organizing clustering , 2005, NeuroImage.

[44]  C. Elger,et al.  Neural Correlates of Successful Declarative Memory Formation and Retrieval: The Anatomical Overlap , 2004, Cortex.

[45]  E. Formisano,et al.  Functional connectivity as revealed by spatial independent component analysis of fMRI measurements during rest , 2004, Human brain mapping.

[46]  A. Georgopoulos,et al.  The internal structure of the phenomenology of auditory verbal hallucinations , 2003, Schizophrenia Research.

[47]  G. Egan,et al.  Cortical activation associated with the experience of auditory hallucinations and perception of human speech in schizophrenia: a PET correlation study , 2003, Psychiatry Research: Neuroimaging.

[48]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[49]  Rainer Goebel,et al.  Cortex-based independent component analysis of fMRI time-series , 2001, NeuroImage.

[50]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[51]  R. Murray,et al.  Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging. , 2000, Archives of general psychiatry.

[52]  I. Aharon,et al.  Three‐dimensional mapping of cortical thickness using Laplace's Equation , 2000, Human brain mapping.

[53]  Erkki Oja,et al.  Independent component analysis: algorithms and applications , 2000, Neural Networks.

[54]  R. Coppola,et al.  Schizophrenia: reduced signal-to-noise ratio and impaired phase-locking during information processing , 2000, Clinical Neurophysiology.

[55]  W. Singer,et al.  Activation of Heschl’s Gyrus during Auditory Hallucinations , 1999, Neuron.

[56]  D. Ffytche,et al.  The anatomy of conscious vision: an fMRI study of visual hallucinations , 1998, Nature Neuroscience.

[57]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[58]  E. Bullmore,et al.  Auditory hallucinations and the temporal cortical response to speech in schizophrenia: a functional magnetic resonance imaging study. , 1997, The American journal of psychiatry.

[59]  Edward T. Bullmore,et al.  Auditory hallucinations inhibit exogenous activation of auditory association cortex , 1996, Neuroreport.

[60]  Richard S. J. Frackowiak,et al.  A functional neuroanatomy of hallucinations in schizophrenia , 1995, Nature.

[61]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[62]  O. Wolkowitz,et al.  High prevalence of visual hallucinations in research subjects with chronic schizophrenia. , 1989, The American journal of psychiatry.

[63]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[64]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[65]  L. M. Graves,et al.  What is a Functional , 1948 .

[66]  D. Prvulovic,et al.  Association between psychotic symptoms and cortical thickness reduction across the schizophrenia spectrum. , 2013, Cerebral cortex.

[67]  D. Pins,et al.  Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. , 2011, The American journal of psychiatry.

[68]  ChrisD . Frith,et al.  Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia , 2009, Nature Reviews Neuroscience.

[69]  Adrian Preda,et al.  Tuning in to the voices: a multisite FMRI study of auditory hallucinations. , 2009, Schizophrenia bulletin.

[70]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[71]  K. Diederen The hallucinating brain , 2008 .

[72]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[73]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[74]  T. Hergueta,et al.  The mini international neuropsychiatric interview , 1998, European Psychiatry.

[75]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[76]  H. Ey Traité des hallucinations , 1973 .

[77]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .